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      Gating and control of primary visual cortex by pulvinar

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          Abstract

          The primary visual cortex (V1) receives its driving input from the eyes via the lateral geniculate nucleus (LGN) of the thalamus. The lateral pulvinar nucleus of the thalamus also projects to V1 but this input is little understood. We manipulated lateral pulvinar neural activity and assessed the effect on supra-granular layers of V1 that project to higher visual cortex. Reversibly inactivating lateral pulvinar prevented supra-granular V1 neurons from responding to visual stimulation. Reversible, focal excitation of lateral pulvinar receptive fields increased 4-fold the visual responses in coincident V1 receptive fields and shifted partially overlapping V1 receptive fields towards the center of excitation. V1 responses to regions surrounding the excited lateral pulvinar receptive fields were suppressed. LGN responses were unaffected by these lateral pulvinar manipulations. Excitation of lateral pulvinar after LGN lesion activated supra-granular layer V1 neurons. Thus, lateral pulvinar is able to powerfully control and gate information outflow from V1.

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          The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs.

          WR Softky, C. Koch (1993)
          How random is the discharge pattern of cortical neurons? We examined recordings from primary visual cortex (V1; Knierim and Van Essen, 1992) and extrastriate cortex (MT; Newsome et al., 1989a) of awake, behaving macaque monkey and compared them to analytical predictions. For nonbursting cells firing at sustained rates up to 300 Hz, we evaluated two indices of firing variability: the ratio of the variance to the mean for the number of action potentials evoked by a constant stimulus, and the rate-normalized coefficient of variation (Cv) of the interspike interval distribution. Firing in virtually all V1 and MT neurons was nearly consistent with a completely random process (e.g., Cv approximately 1). We tried to model this high variability by small, independent, and random EPSPs converging onto a leaky integrate-and-fire neuron (Knight, 1972). Both this and related models predicted very low firing variability (Cv < 1) for realistic EPSP depolarizations and membrane time constants. We also simulated a biophysically very detailed compartmental model of an anatomically reconstructed and physiologically characterized layer V cat pyramidal cell (Douglas et al., 1991) with passive dendrites and active soma. If independent, excitatory synaptic input fired the model cell at the high rates observed in monkey, the Cv and the variability in the number of spikes were both very low, in agreement with the integrate-and-fire models but in strong disagreement with the majority of our monkey data. The simulated cell only produced highly variable firing when Hodgkin-Huxley-like currents (INa and very strong IDR) were placed on distal dendrites. Now the simulated neuron acted more as a millisecond-resolution detector of dendritic spike coincidences than as a temporal integrator. We argue that neurons that act as temporal integrators over many synaptic inputs must fire very regularly. Only in the presence of either fast and strong dendritic nonlinearities or strong synchronization among individual synaptic events will the degree of predicted variability approach that of real cortical neurons.
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            Information processing in the primate visual system: an integrated systems perspective.

            D C Van Essen, C Anderson, D J Felleman (1992)
            The primate visual system contains dozens of distinct areas in the cerebral cortex and several major subcortical structures. These subdivisions are extensively interconnected in a distributed hierarchical network that contains several intertwined processing streams. A number of strategies are used for efficient information processing within this hierarchy. These include linear and nonlinear filtering, passage through information bottlenecks, and coordinated use of multiple types of information. In addition, dynamic regulation of information flow within and between visual areas may provide the computational flexibility needed for the visual system to perform a broad spectrum of tasks accurately and at high resolution.
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              Specificity of monosynaptic connections from thalamus to visual cortex.

              R. P. Reid, Wladmir J. Alonso (1995)
              In cortical area 17 of the cat, simple receptive fields are arranged in elongated subregions that respond best to bright (on) or dark (off) oriented contours, whereas the receptive fields of their thalamic inputs have a concentric on and off organization. This dramatic transformation suggests that there are specific rules governing the connections made between thalamic and cortical neurons (see ref. 4). Here we report a study of these rules in which we recorded from thalamic (lateral geniculate nucleus; LGN) and cortical neurons simultaneously and related their receptive fields to their connectivity, as measured by cross-correlation analysis. The probability of finding a monosynaptic connection was high when a geniculate receptive field was superimposed anywhere over an elongated simple-cell subregion of the same signature (on or off). However, 'inappropriate' connections from geniculate cells of the opposite receptive field signature were extremely rare. Together, these findings imply that the outline of the elongated, simple receptive field, and thus of cortical orientation selectivity, is laid down at the level of the first synapse from the thalamic afferents.
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                Author and article information

                Journal
                Journal ID (nlm-journal-id): 9809671
                Journal ID (pubmed-jr-id): 21092
                Journal ID (nlm-ta): Nat Neurosci
                Journal ID (iso-abbrev): Nat. Neurosci.
                Title: Nature neuroscience
                ISSN (Print): 1097-6256
                ISSN (Electronic): 1546-1726
                Publication date Nihms-submitted: 20 April 2012
                Publication date (Print): June 2012
                Publication date PMC-release: 01 December 2012
                Volume: 15
                Issue: 6
                Pages: 905-912
                Affiliations
                [1 ]Department of Cell and Developmental Biology, Vanderbilt University
                [2 ]Department of Psychology, Vanderbilt University
                Article
                Manuscript ID: NIHMS369780
                DOI: 10.1038/nn.3106
                PMC ID: 3430824
                PubMed ID: 22561455
                SO-VID: 6636e40a-da5f-4090-974b-a560ebbc8ce8
                License:

                Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

                History
                Funding
                Funded by: National Institute of Child Health & Human Development : NICHD
                Award ID: P30 HD015052-32 || HD
                Funded by: National Eye Institute : NEI
                Award ID: P30 EY008126-24 || EY
                Categories
                Subject: Article

                ScienceOpen disciplines: Neurosciences
                Data availability:
                ScienceOpen disciplines: Neurosciences

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